Transcriptomic Response to Perkinsus marinus in Two Crassostrea Oysters Reveals Evolutionary Dynamics of Host-Parasite Interactions

Abstract

Infectious disease outbreaks are causing widespread declines of marine invertebrates including corals, sea stars, shrimps, and molluscs. Dermo is a lethal infectious disease of the eastern oyster Crassostrea virginica caused by the protist Perkinsus marinus. The Pacific oyster Crassostrea gigas is resistant to Dermo due to differences in the host-parasite interaction that is not well understood. We compared transcriptomic responses to P. marinus challenge in the two oysters at early and late infection stages. Dynamic and orchestrated regulation of large sets of innate immune response genes were observed in both species with remarkably similar patterns for most orthologs, although responses in C. virginica were stronger, suggesting strong or over-reacting immune response could be a cause of host mortality. Between the two species, several key immune response gene families differed in their expansion, sequence variation and/or transcriptional response to P. marinus, reflecting evolutionary divergence in host-parasite interaction. Of note, significant upregulation of inhibitors of apoptosis (IAPs) was observed in resistant C. gigas but not in susceptible C. virginica, suggesting upregulation of IAPs is an active defense mechanism, not a passive response orchestrated by P. marinus. Compared with C. gigas, C. virginica exhibited greater expansion of toll-like receptors (TLRs) and positive selection in P. marinus responsive TLRs. The C1q domain containing proteins (C1qDCs) with the galactose-binding lectin domain that is involved in P. marinus recognition, were only present and significantly upregulated in C. virginica. These results point to previously undescribed differences in host defense genes between the two oyster species that may account for the difference in susceptibility, providing an expanded portrait of the evolutionary dynamics of host-parasite interaction in lophotrochozoans that lack adaptive immunity. Our findings suggest that C. virginica and P. marinus have a history of coevolution and the recent outbreaks may be due to increased virulence of the parasite.

Chromosomal assembly of the flat oyster (Ostrea edulis L.) genome as a new genetic resource for aquaculture

“…On the contrary, the high number of differentially regulated genes and corresponding biological functions in the digestive gland emphasizes the systemic response of O. edulis to M. refringens . In hemocytes, a downregulation occurred for genes encoding IAPs, mannose receptor C‐type, serine protease inhibitor, and C1q complement that all contribute to the molecular response to parasites (Chan et al, 2021 ; Li et al, 2019 ). In the digestive gland, 11 genes coding for C1q different from those identified in hemocytes are instead upregulated demonstrating differential regulation of this protein family.…”

Chromosomal assembly of the flat oyster (Ostrea edulisL.) genome as a new genetic ressource for aquaculture

“…This first study carried out on individuals naturally infected by M. refringens , although preliminary, allowed to highlight some metabolic pathways classicaly involved in parsite interaction but also new pathways that could be more specifically associated to the response to a eukaryote parasite. Indeed, in hemocytes, the main tissue involved in immune response, the down-regulation of genes such as IAPs, mannose receptor C-type, serine protease inhibitor, and C1q complement that participate to the molecular response to various parasites (Li et al, 2019; Chan et al, 2021). The down-regulation of those genes could indicate a lower capacity of immune response by the oyster.…”

Transcriptomic Response of the Atlantic Surfclam (Spisula solidissima) to Acute Heat Stress

“…While both groups expressed genes that promote apoptosis at 29 °C, the induction of apoptosis was likely largely mitigated because both HS and RC clams significantly upregulated between 30 and 50 inhibitors of apoptosis (IAPs). Significant upregulation of an expanded set of IAPs is a key feature of stress (Zhang et al 2012a, b;Guo et al 2015;Song et al 2021) and immune (He et al 2015;Chan et al 2021;Witkop et al 2022) responses in bivalve mollusks. While the RC group expressed more IAPs, the HS group exhibited a stronger response; the HS group exhibiting a 50-fold increase in IAP expression, while the RC group had only a 19-fold increase.…”